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Control of mammary stem cell function by steroid hormone signalling
Abstract
The ovarian hormones oestrogen and progesterone profoundly influence breast cancer risk, underpinning the benefit of endocrine therapies in the treatment of breast cancer. Modulation of their effects through ovarian ablation or chemoprevention strategies also significantly decreases breast cancer incidence. Conversely, there is an increased risk of breast cancer associated with pregnancy in the short term. The cellular mechanisms underlying these observations, however, are poorly defined. Here we demonstrate that mouse mammary stem cells (MaSCs) are highly responsive to steroid hormone signalling, despite lacking the oestrogen and progesterone receptors. Ovariectomy markedly diminished MaSC number and outgrowth potential in vivo, whereas MaSC activity increased in mice treated with oestrogen plus progesterone. Notably, even three weeks of treatment with the aromatase inhibitor letrozole was sufficient to reduce the MaSC pool. In contrast, pregnancy led to a transient 11-fold increase in MaSC numbers, probably mediated through paracrine signalling from RANK ligand. The augmented MaSC pool indicates a cellular basis for the short-term increase in breast cancer incidence that accompanies pregnancy. These findings further indicate that breast cancer chemoprevention may be achieved, in part, through suppression of MaSC function.
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“It is therefore especially useful for finding similarities in gene expression patterns between different expression studies (57,59–61) (Figure 4C).”
From limma powers differential expression analyses for RNA-sequencing and microarray studies (2015) · cites this paper as [61]
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“We also found that RANK and RANKL expression differ according to the pregnancy trimester (Additional file 2), which was also observed in preclinical experiments [4].”
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“supported by the fact that MaSCs pool increases during the luteal diestrus phase and throughout pregnancy [56, 57].”
BackgroundInfluentialOvarian steroids, stem cells and uterine leiomyoma: therapeutic implications
Moravek, M. B., Yin, P., Ono, M., Coon, J. S., Dyson, M. T., Navarro, A., Marsh, E. E., Chakravarti, D., Kim, J. J., Wei, J., et al. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu048 · Cited by 158
“Scientific direction may be taken from the breast cancer literature, which is a better-studied model of stem-progenitor cells that are deficient in ERs and PRs, but are hormone responsive via paracrine interaction with surrounding differentiated cells (Asselin-Labat et al., 2010; Fillmore et al., 2010; Roarty and Rose…”
BackgroundCicchini, M., Chakrabarti, R., Kongara, S., Price, S. M., Nahar, R., Lozy, F., Zhong, H., Vázquez, A., Kang, Y., & Karantza, V. (2014) · Autophagy · doi:10.4161/auto.34398 · Cited by 159
“For ovariectomization and stimulation studies procedures were performed as previously described.(32)”
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“The adult mammary gland seems to harbour multiple stem cell populations, including slow-cycling 43 or putative quiescent MaSCs 44,45 , as well as a molecularly distinct MaSC subset that transiently expands during pregnancy 46 .”
Self-citationTamoxifen and Risk of Contralateral Breast Cancer for BRCA1 and BRCA2 Mutation Carriers
Phillips, K.-A., Milne, R. L., Rookus, M. A., Daly, M. B., Antoniou, A. C., Peock, S., Frost, D., Easton, D. F., Ellis, S., Friedlander, M. L., et al. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.47.8313 · Cited by 171
Leeuwen, I. J. D. V.-V., Pereira, D. D. C., Flach, K. D., Piersma, S. R., Haase, C., Bier, D., Yalçin, Z., Michalides, R. J. A. M., Feenstra, K. A., Jiménez, C. R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220809110 · Cited by 148
“Current therapeutic strategies to treat these tumors rely on selective ER modulators (SERMs), like tamoxifen (TAM) (1) or aromatase inhibitors (AIs) that block estradiol synthesis (2).”
BackgroundHilton, H. N., Clarke, C. L., & Graham, J. D. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.08.011 · Cited by 158
Impact of risk factors on early cancer evolution
Weeden, C. E., Hill, W., Lim, E. L., Gronroos, E. C., & Swanton, C. (2023) · Cell · doi:10.1016/j.cell.2023.03.013 · Cited by 147
Role of stem cells in human uterine leiomyoma growth
Ono, M., Qiang, W., Serna, V. A., Yin, P., Coon, J. S., Navarro, A., Monsivais, D., Kakinuma, T., Dyson, M., Druschitz, S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036935 · Cited by 141
“In mammary structures of humans and mice, mammary stem cells, despite being void of ESR1 and PGR themselves, are subject to regulation in both number and repopulating ability by steroid hormones, particularly progesterone [40,41,42,43].”
BackgroundWnt/β-catenin Signaling in Normal and Cancer Stem Cells
Valkenburg, K. C., Graveel, C. R., Diegel, C. R., Zhong, Z. A., & Williams, B. O. (2011) · Cancers · doi:10.3390/cancers3022050 · Cited by 144
“In mice MaSCs are highly enriched in the CD49f hi CD29 hi CD24 + Sca1 - subpopulation [103-105], whereas human cells with features of MaSCs have been identified in the CD49f hi EpCAM - subpopulation [106,107].”
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Azim, H. A., Nguyen, B., Brohée, S., Zoppoli, G. M., & Sotiriou, C. P. (2015) · BMC Medicine · doi:10.1186/s12916-015-0504-3 · Cited by 140
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“In addition, it has been reported that endogenous progesterone affects the numbers of Lin-CD24+CD49f mammary epithelial stem cells during pregnancy [69] and during the 650 J Mol Med (2011) 89:647–656”
BackgroundIdentification of quiescent and spatially restricted mammary stem cells that are hormone responsive
Fu, N. Y., Rios, A. C., Pal, B., Law, C. W., Jamieson, P. R., Liu, R., Vaillant, F., Jackling, F. C., Liu, K. H., Smyth, G. K., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3471 · Cited by 141
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“Recent studies have identified an important role for progesterone in regulating the number of stem cells in normal human and mouse mammary glands [25,26].”
BackgroundGlobal Changes in the Mammary Epigenome Are Induced by Hormonal Cues and Coordinated by Ezh2
Pal, B., Bouras, T., Shi, W., Vaillant, F., Sheridan, J. M., Fu, N. Y., Breslin, K. A., Jiang, K., Ritchie, M. E., Young, M. D., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2012.12.020 · Cited by 134
“However, the changes apparent in cell cycle regulators may suffice to drive MaSCs into a more quiescent state, as indicated by molecular profiling and cellular analyses (Asselin-Labat et al., 2010).”
BackgroundInfluentialForm and Function: how Estrogen and Progesterone Regulate the Mammary Epithelial Hierarchy
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“Treatment of mice with the aromatase inhibitor letrozole significantly diminishes repopulating cell numbers [125].”
BackgroundRitte, R., Lukanova, A., Berrino, F., Dossus, L., Tjønneland, A. M., Olsen, A., Overvad, T. F., Overvad, K., Clavel‐Chapelon, F., Fournier, A., et al. (2012) · Breast Cancer Research · doi:10.1186/bcr3186 · Cited by 129
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Cittelly, D. M., Finlay-Schultz, J., Howe, E. N., Spoelstra, N. S., Axlund, S. D., Hendricks, P., Jacobsen, B. M., Sartorius, C. A., & Richer, J. K. (2012) · Oncogene · doi:10.1038/onc.2012.275 · Cited by 126
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Manavathi, B., Dey, O., Gajulapalli, V. N. R., Bhatia, R. S., Bugide, S., & Kumar, R. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1057 · Cited by 131
“creased in mice treated with E2 plus progesterone (291).”
BackgroundReproductive history and breast cancer risk
Kobayashi, S., Sugiura, H., Ando, Y., Shiraki, N., Yanagi, T., Yamashita, H., & Toyama, T. (2012) · Breast Cancer · doi:10.1007/s12282-012-0384-8 · Cited by 123
“were clarified by 2 different groups [36, 37] (Fig.”
BackgroundAyyanan, A., Laribi, O., Schuepbach‐Mallepell, S., Schrick, C., Gutierrez, M. J., Tanos, T., Lefebvre, G. C., Rougemont, J., Yalcin-Ozuysal, Ö., & Brisken, C. (2011) · Molecular Endocrinology · doi:10.1210/me.2011-1129 · Cited by 123
From milk to malignancy: the role of mammary stem cells in development, pregnancy and breast cancer
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Common Breast Cancer Susceptibility Loci Are Associated with Triple-Negative Breast Cancer
Purrington, K. S., Vachon, C. M., Lee, A. M., Slager, S., Lesnick, T. G., Olswold, C., Fasching, P. A., Miron, P. L., Eccles, D., Carpenter, J., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1266 · Cited by 119
“However, recent studies in mice have shown that the mammary stem cell compartment can be regulated by 17 く-estradiol and progesterone through a paracrine-signalling mechanism from steroid receptor-positive luminal cells to steroid receptor-negative stem cells (29, 30).”
The RANK–RANKL–OPG System: A Multifaceted Regulator of Homeostasis, Immunity, and Cancer
León-Oliva, D. D., Barrena-Blázquez, S., Jiménez-Álvarez, L., Fraile‐Μartinez, O., Montero, C. G., López-González, L., Torres‐Carranza, D., García-Puente, L. M., Carranza, S. T., Álvarez-Mon, M. Á., et al. (2023) · Medicina · doi:10.3390/medicina59101752 · Cited by 153
“RANKL then engages with RANK in both an autocrine and paracrine fashion, thereby stimulating cellular proliferation, including the pool of mammary stem cells, and the formation of milk-secreting acini throughout pregnancy (Figure 2) [44,45].”
BackgroundGarbe, J. C., Pepin, F., Pelissier, F. A., Sputova, K., Fridriksdottir, A. J., Guo, D. E., Villadsen, R., Park, M., Petersen, O. W., Borowsky, A. D., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-0157 · Cited by 123
“Estrogen and progesterone can directly impact the epithelium by causing fluctuations in the stem cell pool (8, 9) and are required for gland morphogenesis (10–12).”
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“Other pathways associated with mammary stem/progenitor cells and mammary gland development [39–41], such as Wnt/b-catenin and RANK signaling pathways were also implicated in the gene expression patterns.”
HER2 and Breast Cancer Stem Cells: More than Meets the Eye
Körkaya, H., & Wicha, M. S. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-0260 · Cited by 120
“It has previously been shown that normal breast stem cells are regulated by RANK ligand, which is produced in response to progesterone elevation during pregnancy (21, 22).”
BackgroundMammary Development and Breast Cancer: A Wnt Perspective
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“RANKL (receptor activator of NF-kB ligand) is another downstream target of progesterone that has been proposed to be a hormone-mediated local factor for MaSCs [139].”
BackgroundWnt and Neuregulin1/ErbB signalling extends 3D culture of hormone responsive mammary organoids
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Estrogen and Progesterone in Normal Mammary Gland Development and in Cancer
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“The effects of reduced exposure to estrogen on MRUs are thought to be mediated by inducing these cells into a quiescent state [ 32 ].”
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“Recent evidence indicates a special role of steroid hormones in the control of normal mammary stem cell function (24, 25) that implicates stem cells as the potential target during hormonal carcinogenesis.”
BackgroundMammary Stem Cells: Premise, Properties, and Perspectives
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Metadata
- Authors
- Asselin-Labat, M.-L., Vaillant, F., Sheridan, J. M., Pal, B., Wu, D., Simpson, E. R., Yasuda, H., Smyth, G. K., Martin, T. J., Lindeman, G. J., & Visvader, J. E.
- Affiliations
- Walter and Eliza Hall Institute of Medical Research (AU)
- The University of Melbourne (AU)
- Monash Medical Centre (AU)
- Oriental Yeast Co., Ltd. (Japan) (JP)
- St Vincents Institute of Medical Research (AU)
- The Royal Melbourne Hospital (AU)
- Corresponding author
- Lindeman, Geoffrey J.
- Visvader, Jane E.
- ORCID
- Venue
- Nature
- Published
- 2010-04-11
- Volume
- 465
- Issue
- 7299
- Pages
- 798-802
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2117963341
- Cited by
- 693
- References
- 38
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 29 · 2023: 22 · 2022: 29 · 2021: 30 · 2020: 30 · 2019: 32 · 2018: 40 · 2017: 44 · 2016: 45 · 2015: 63 · 2014: 53 · 2013: 64 · 2012: 76
- FWCI
- 45.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
- Keywords
- mammary stem cells, steroid hormone signaling, estrogen, progesterone, RANKL, breast cancer risk, pregnancy, ovariectomy, letrozole, aromatase inhibition, chemoprevention, paracrine signaling, mammary gland development
- MeSH terms
- Letrozole, Animals, Aromatase, Cell Count, Estrogens, Female, Humans, Mammary Glands, Animal, Nitriles, Ovariectomy, Pregnancy, Pregnancy, Animal, Progesterone, Receptors, Estrogen, Receptors, Progesterone, Stem Cells, Triazoles, Signal Transduction, Integrin beta1, Paracrine Communication, Integrin beta3, Aromatase Inhibitors, Mice, CD24 Antigen, RANK Ligand, ErbB Receptors
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